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Hyaluronidase of bloodsucking insects and its enhancing effect on leishmania infection in mice.

Volfova V, Hostomska J, Cerny M, Votypka J, Volf P - PLoS Negl Trop Dis (2008)

Bottom Line: No activity was found in kissing bug Rhodnius prolixus, mosquitoes Anopheles stephensi and Aedes aegypti, tse-tse fly Glossina fuscipes, stable fly Stomoxys calcitrans and human louse Pediculus humanus.Hyaluronidases of different insects vary substantially in their molecular weight, the structure of the molecule and the sensitivity to reducing conditions or sodium dodecyl sulphate.As this enzyme is present in all Phlebotomus and Lutzomyia species studied to date, it seems to be one of the factors responsible for enhancing activity present in sand fly saliva.

View Article: PubMed Central - PubMed

Affiliation: Department of Parasitology, Faculty of Science, Charles University in Prague, Czech Republic. volf@cesnet.cz

ABSTRACT

Background: Salivary hyaluronidases have been described in a few bloodsucking arthropods. However, very little is known about the presence of this enzyme in various bloodsucking insects and no data are available on its effect on transmitted microorganisms. Here, we studied hyaluronidase activity in thirteen bloodsucking insects belonging to four different orders. In addition, we assessed the effect of hyaluronidase coinoculation on the outcome of Leishmania major infection in BALB/c mice.

Principal findings: High hyaluronidase activity was detected in several Diptera tested, namely deer fly Chrysops viduatus, blackflies Odagmia ornata and Eusimilium latipes, mosquito Culex quinquefasciatus, biting midge Culicoides kibunensis and sand fly Phlebotomus papatasi. Lower activity was detected in cat flea Ctenocephalides felis. No activity was found in kissing bug Rhodnius prolixus, mosquitoes Anopheles stephensi and Aedes aegypti, tse-tse fly Glossina fuscipes, stable fly Stomoxys calcitrans and human louse Pediculus humanus. Hyaluronidases of different insects vary substantially in their molecular weight, the structure of the molecule and the sensitivity to reducing conditions or sodium dodecyl sulphate. Hyaluronidase exacerbates skin lesions caused by Leishmania major; more severe lesions developed in mice where L. major promastigotes were coinjected with hyaluronidase.

Conclusions: High hyaluronidase activities seem to be essential for insects with pool-feeding mode, where they facilitate the enlargement of the feeding lesion and serve as a spreading factor for other pharmacologically active compounds present in saliva. As this enzyme is present in all Phlebotomus and Lutzomyia species studied to date, it seems to be one of the factors responsible for enhancing activity present in sand fly saliva. We propose that salivary hyaluronidase may facilitate the spread of other vector-borne microorganisms, especially those transmitted by insects with high hyaluronidase activity, namely blackflies (Simuliidae), biting midges (Ceratopogonidae) and horse flies (Tabanidae).

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SDS PAGE zymography on the same gel as in Figure 3 but under reducing conditions.Pp = Phlebotomus papatasi SGE (0.2 µg), Ck = Culicoides kibunensis BE (20 µg), Cq = Culex quinquefasciatus SGE (8 µg), El = Eusimulium latipes SGE (3 µg), Oo = Odagmia ornata SGE (3 µg), Cv = Chrysops viduatus SGE (0.3 µg), Cf = Ctenocephalides felis BE (15 µg).
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pntd-0000294-g004: SDS PAGE zymography on the same gel as in Figure 3 but under reducing conditions.Pp = Phlebotomus papatasi SGE (0.2 µg), Ck = Culicoides kibunensis BE (20 µg), Cq = Culex quinquefasciatus SGE (8 µg), El = Eusimulium latipes SGE (3 µg), Oo = Odagmia ornata SGE (3 µg), Cv = Chrysops viduatus SGE (0.3 µg), Cf = Ctenocephalides felis BE (15 µg).

Mentions: Seven samples positive in the dot method were analyzed by zymography to reveal the apparent molecular weight (MW) of hyaluronidases. The MW of the enzymes differed among various insects (Figs. 3 and 4). Under nonreducing conditions hyaluronidases were detected as major diffuse bands (Fig. 3). The SGE activity in Phlebotomus papatasi had a MW about 70 kDa while those in both blackfly species tested, Eusimulium latipes, and Odagmia ornata, about 40 kDa. In BE of Culicoides kibunensis, the major band of about 35 kDa was accompanied with a minor one of 70 kDa, supposedly a dimer. Chrysops viduatus SGE revealed one major band with estimated MW of 50 kDa. In BE of flea Ctenocephalides felis, three enzyme bands were detected, the most prominent one of about 52 kDa (Fig. 3). Under reducing conditions, SDS PAGE revealed sharper enzyme bands allowing more precise assignment of corresponding MW (Fig. 4). In sand fly P. papatasi, both blackfly species and deer fly Chrysops viduatus, hyaluronidase activity was observed within the same MW ranges as under nonreducing conditions (70, 40 kDa, and 50 kDa, respectively). In Culicoides kibunensis and Ctenocephalides felis hyaluronidase activity was not detectable under reducing conditions (Fig. 4).


Hyaluronidase of bloodsucking insects and its enhancing effect on leishmania infection in mice.

Volfova V, Hostomska J, Cerny M, Votypka J, Volf P - PLoS Negl Trop Dis (2008)

SDS PAGE zymography on the same gel as in Figure 3 but under reducing conditions.Pp = Phlebotomus papatasi SGE (0.2 µg), Ck = Culicoides kibunensis BE (20 µg), Cq = Culex quinquefasciatus SGE (8 µg), El = Eusimulium latipes SGE (3 µg), Oo = Odagmia ornata SGE (3 µg), Cv = Chrysops viduatus SGE (0.3 µg), Cf = Ctenocephalides felis BE (15 µg).
© Copyright Policy
Related In: Results  -  Collection

Show All Figures
getmorefigures.php?uid=PMC2553483&req=5

pntd-0000294-g004: SDS PAGE zymography on the same gel as in Figure 3 but under reducing conditions.Pp = Phlebotomus papatasi SGE (0.2 µg), Ck = Culicoides kibunensis BE (20 µg), Cq = Culex quinquefasciatus SGE (8 µg), El = Eusimulium latipes SGE (3 µg), Oo = Odagmia ornata SGE (3 µg), Cv = Chrysops viduatus SGE (0.3 µg), Cf = Ctenocephalides felis BE (15 µg).
Mentions: Seven samples positive in the dot method were analyzed by zymography to reveal the apparent molecular weight (MW) of hyaluronidases. The MW of the enzymes differed among various insects (Figs. 3 and 4). Under nonreducing conditions hyaluronidases were detected as major diffuse bands (Fig. 3). The SGE activity in Phlebotomus papatasi had a MW about 70 kDa while those in both blackfly species tested, Eusimulium latipes, and Odagmia ornata, about 40 kDa. In BE of Culicoides kibunensis, the major band of about 35 kDa was accompanied with a minor one of 70 kDa, supposedly a dimer. Chrysops viduatus SGE revealed one major band with estimated MW of 50 kDa. In BE of flea Ctenocephalides felis, three enzyme bands were detected, the most prominent one of about 52 kDa (Fig. 3). Under reducing conditions, SDS PAGE revealed sharper enzyme bands allowing more precise assignment of corresponding MW (Fig. 4). In sand fly P. papatasi, both blackfly species and deer fly Chrysops viduatus, hyaluronidase activity was observed within the same MW ranges as under nonreducing conditions (70, 40 kDa, and 50 kDa, respectively). In Culicoides kibunensis and Ctenocephalides felis hyaluronidase activity was not detectable under reducing conditions (Fig. 4).

Bottom Line: No activity was found in kissing bug Rhodnius prolixus, mosquitoes Anopheles stephensi and Aedes aegypti, tse-tse fly Glossina fuscipes, stable fly Stomoxys calcitrans and human louse Pediculus humanus.Hyaluronidases of different insects vary substantially in their molecular weight, the structure of the molecule and the sensitivity to reducing conditions or sodium dodecyl sulphate.As this enzyme is present in all Phlebotomus and Lutzomyia species studied to date, it seems to be one of the factors responsible for enhancing activity present in sand fly saliva.

View Article: PubMed Central - PubMed

Affiliation: Department of Parasitology, Faculty of Science, Charles University in Prague, Czech Republic. volf@cesnet.cz

ABSTRACT

Background: Salivary hyaluronidases have been described in a few bloodsucking arthropods. However, very little is known about the presence of this enzyme in various bloodsucking insects and no data are available on its effect on transmitted microorganisms. Here, we studied hyaluronidase activity in thirteen bloodsucking insects belonging to four different orders. In addition, we assessed the effect of hyaluronidase coinoculation on the outcome of Leishmania major infection in BALB/c mice.

Principal findings: High hyaluronidase activity was detected in several Diptera tested, namely deer fly Chrysops viduatus, blackflies Odagmia ornata and Eusimilium latipes, mosquito Culex quinquefasciatus, biting midge Culicoides kibunensis and sand fly Phlebotomus papatasi. Lower activity was detected in cat flea Ctenocephalides felis. No activity was found in kissing bug Rhodnius prolixus, mosquitoes Anopheles stephensi and Aedes aegypti, tse-tse fly Glossina fuscipes, stable fly Stomoxys calcitrans and human louse Pediculus humanus. Hyaluronidases of different insects vary substantially in their molecular weight, the structure of the molecule and the sensitivity to reducing conditions or sodium dodecyl sulphate. Hyaluronidase exacerbates skin lesions caused by Leishmania major; more severe lesions developed in mice where L. major promastigotes were coinjected with hyaluronidase.

Conclusions: High hyaluronidase activities seem to be essential for insects with pool-feeding mode, where they facilitate the enlargement of the feeding lesion and serve as a spreading factor for other pharmacologically active compounds present in saliva. As this enzyme is present in all Phlebotomus and Lutzomyia species studied to date, it seems to be one of the factors responsible for enhancing activity present in sand fly saliva. We propose that salivary hyaluronidase may facilitate the spread of other vector-borne microorganisms, especially those transmitted by insects with high hyaluronidase activity, namely blackflies (Simuliidae), biting midges (Ceratopogonidae) and horse flies (Tabanidae).

Show MeSH
Related in: MedlinePlus